Polynoidae is the most diverse radiation of Aphroditiformia and one of the most successful groups of all Annelida in terms of diversity and habitats colonized. With such an unmatched diversity, phylogenetic investigations have struggled to understand their evolutionary relationships. Previous phylogenetic analyses have slowly increased taxon sampling and employed methodologies, but despite their diversity and biological importance, large genomic sampling is limited. To investigate the internal relationships within Polynoidae, we conducted the first phylogenomic analyses of the group based on 12 transcriptomes collected from species inhabiting a broad array of habitats, including shallow and deep waters, as well as hydrothermal vents, anchialine caves and the midwater. Our phylogenomic analyses of Polynoidae recovered congruent tree topologies representing the clades Polynoinae, Macellicephalinae and Lepidonotopodinae. Members of Polynoinae and Macellicephalinae clustered in well-supported and independent clades. In contrast, Lepidonotopodinae taxa were always recovered nested within Macellicephalinae. Though our sampling only covers a small proportion of the species known for Polynoidae, our results provide a robust phylogenomic framework to build from, emphasizing previously hypothesized relationships between Macellicephalinae and Lepidonotopodinae taxa, while providing new insights on the origin of enigmatic cave and pelagic lineages.